Advertisement

Hydrobiologia

, Volume 687, Issue 1, pp 49–59 | Cite as

The mitochondrial genome of stygobitic sponge Eunapius subterraneus: mtDNA is highly conserved in freshwater sponges

  • Bruna PlešeEmail author
  • Lada Lukić-Bilela
  • Branka Bruvo-Mađarić
  • Matija Harcet
  • Mirna Imešek
  • Helena Bilandžija
  • Helena ĆetkovićEmail author
SPONGE RESEARCH DEVELOPMENTS

Abstract

The complete mitochondrial DNA (mtDNA) genome of the Eunapius subterraneus (Porifera, Demospongiae), a unique stygobitic sponge, was analyzed and compared with previously published mitochondrial genomes from this group. The 24,850 bp long mtDNA genome is circular with the same gene composition as found in other metazoans. Intergenic regions (IGRs) comprise 24.7% of mtDNA and are abundant with direct and inverted repeats and palindromic elements as well as with open reading fames (ORFs) whose distribution and homology was compared with other available mt genomes with a special focus on freshwater sponges. Phylogenetic analyses based on concatenated amino acid sequences from 12 mt protein genes placed E. subterraneus in a well-supported monophyletic clade with the freshwater sponges, Ephydatia muelleri and Lubomirskia baicalensis. Our study showed high homology of mtDNA genomes among freshwater sponges, implying their recent split.

Keywords

Porifera Spongillidae Stygobitic Mitochondrial evolution 

Notes

Acknowledgments

We thank Branko Jalžić and members of the Croatian Biospeleological Society for their help with specimen collection and acknowledge financial support from Croatian MSES grant 098-0982913-2478 (H. Ćetković). Prof. William R. Jeffery is gratefully acknowledged for proofreading the manuscript.

Supplementary material

10750_2011_789_MOESM1_ESM.jpg (2.7 mb)
Supplementary Fig. 1. Secondary structure of trnX from Ephydatia muelleri, Lubomirskia baicalensis, and Eunapius subterraneus with nucleotide identity presented in the table. Nucleotides that differ in comparison with E. subterraneus are marked in red. (JPEG 2738 kb)

References

  1. Abascal, F., R. Zardoya & D. Posada, 2005. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104–2105.PubMedCrossRefGoogle Scholar
  2. Addis, J. S. & K. J. Peterson, 2005. Phylogenetic relationships of freshwater sponges (Porifera, Spongillina) inferred from analyses of 18S rDNA, COI mtDNA, and ITS2 rDNA sequences. Zoologica scripta 34: 549–557.CrossRefGoogle Scholar
  3. Anisimova, M. & O. Gascuel, 2006. Approximate likelihood ratio test for branches: a fast, accurate and powerful alternative. Systematic Biology 55: 539–552.PubMedCrossRefGoogle Scholar
  4. Aono, N., T. Shimizu, T. Inoue & H. Shiraishi, 2002. Palindromic repetitive elements in the mitochondrial genome of Volvox. FEBS Letters 521: 95–99.PubMedCrossRefGoogle Scholar
  5. Arunkumar, K. P. & J. Nagaraju, 2006. Unusually long palindromes are abundant in mitochondrial control regions of insects and nematodes. Plos ONE 1: e110.PubMedCrossRefGoogle Scholar
  6. Basrai, M. A., P. Hieter & J. D. Boeke, 1997. Small open reading frames: beautiful needles in the haystack. Genome Research 7: 768–771.PubMedGoogle Scholar
  7. Belinky, F., C. Rot, M. Ilan & D. Huchon, 2008. The complete mitochondrial genome of the demosponge Negombata magnifica (Poecilosclerida). Molecular Phylogenetics and Evolution 47: 1238–1243.PubMedCrossRefGoogle Scholar
  8. Benson, D. A., I. Karsch-Mizrachi, D. J. Lipman, J. Ostell & D. L. Wheeler, 2003. GenBank. Nucleic Acids Research 31: 23–27.PubMedCrossRefGoogle Scholar
  9. Bilandžija, H., J. Bedek, B. Jalžić & S. Gottstein, 2007. The morphological variability, distribution patterns and endangerment in the Ogulin cave sponge Eunapius subterraneus. Natura Croatica 16: 1–17.Google Scholar
  10. Bilandžija, H., J. Bedek & B. Jalžić, 2009. Ogulin cave sponge. In Ozimec, R., et al. (eds), Red Book of Croatia Cave Dwelling Fauna. Ministry of culture, State Institute for Nature Protection, Zagreb: 176–177.Google Scholar
  11. Boore, J. L., 1999. Animal mitochondrial genomes. Nucleic Acids Research 27: 1767–1780.PubMedCrossRefGoogle Scholar
  12. Borchiellini, C., C. Chombard, M. Manuel, E. Alivon, J. Vacelet & N. Boury-Esnault, 2004. Molecular phylogeny of Demospongiae: implications for classification and scenarios of character evolution. Molecular Phylogenetics and Evolution 32: 823–837.PubMedCrossRefGoogle Scholar
  13. Burger, G., L. Forget, Y. Zhu, M. W. Gray & B. F. Lang, 2003. Unique mitochondrial genome architecture in unicellular relatives of animals. Proceedings of the National Academy of Sciences USA 100: 892–897.CrossRefGoogle Scholar
  14. Castresana, J., 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17: 540–552.PubMedGoogle Scholar
  15. Drummond, A. & K. Strimmer, 2001. PAL: An object-oriented programming library for molecular evolution and phylogenetics. Bioinformatics 17: 662–663.PubMedCrossRefGoogle Scholar
  16. Erpenbeck, D., O. Voigt, M. Adamski, M. Adamska, J. N. A. Hooper, G. Wörheide & B. M. Degnan, 2007. Mitochondrial diversity of early-branching metazoa is revealed by the complete mt genome of a Haplosclerid Demosponge. Molecular Biology and Evolution 24: 19–22.PubMedCrossRefGoogle Scholar
  17. Erpenbeck, D., O. Voigt, G. Wörheide & D. V. Lavrov, 2009. The mitochondrial genomes of sponges provide evidence for multiple invasions by repetitive hairpin-forming elements (RHE). BMC Genomics 10: 591.PubMedCrossRefGoogle Scholar
  18. Flot, J. F. & S. Tillier, 2007. The mitochondrial genome of Pocillopora (Cnidaria: Scleractinia) contains two variable regions: the putative D-loop and a novel ORF of unknown function. Gene 401: 80–87.PubMedCrossRefGoogle Scholar
  19. Guindon, S. & O. Gascuel, 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52: 696–704.PubMedCrossRefGoogle Scholar
  20. Harcet, M., H. Bilandžija, B. Bruvo-Mađarić & H. Ćetković, 2010. Taxonomic position of Eunapius subterraneus (Porifera, Spongillidae) inferred from molecular data—a revised classification needed? Molecular Phylogenetics and Evolution 54: 1021–1027.PubMedCrossRefGoogle Scholar
  21. Hixson, J. E., T. W. Wong & D. A. Clayton, 1986. Both the conserved stem-loop and divergent 59-flanking sequences are required for initiation at the human mitochondrial origin of light-strand DNA replication. The Journal of Biological Chemistry 261: 2384–2390.PubMedGoogle Scholar
  22. Hooper, J. N. A. & R. W. M. van Soest, 2002. Class Demospongiae Sollas, 1885. In Hooper, J. N. A. & R. W. M. van Soest (eds), Systema Porifera: A guide to the Classification of Sponges. Kluwer, New York: 15–18.Google Scholar
  23. Huelsenbeck, J. P. & F. Ronquist, 2001. MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17: 754–755.PubMedCrossRefGoogle Scholar
  24. Kastenmayer, J. P., L. Ni, A. Chu, L. E. Kitchen, W. C. Au, H. Yang, C. D. Carter, D. Wheeler, R. W. Davis, J. D. Boeke, M. A. Snyder & M. A. Basrai, 2006. Functional genomics of genes with small open reading frames (sORFs) in S. cerevisiae. Genome Research 16: 365–373.PubMedCrossRefGoogle Scholar
  25. Kornberg, A. & T. Baker, 1992. DNA Replication. W. Freeman & Co, New York.Google Scholar
  26. Lavrov, D. V., 2007. Key transitions in animal evolution: a mitochondrial DNA perspective. Integrative and Comparative Biology 47: 734–743.PubMedCrossRefGoogle Scholar
  27. Lavrov, D. V., 2009. Rapid proliferation of repetitive palindromic elements in mtDNA of the endemic Baikalian sponge Lubomirskia baicalensis. Molecular Biology and Evolution. doi:10.1093/molbev/msp317.
  28. Lavrov, D. V., L. Forget, M. Kelly & B. F. Lang, 2005. Mitochondrial genomes of two demosponges provide insights into an early stage of animal evolution. Molecular Biology and Evolution 22: 1231–1239.PubMedCrossRefGoogle Scholar
  29. Lowe, T. M. & S. R. Eddy, 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Research 31: 176–178.Google Scholar
  30. Lukić-Bilela, L., D. Brandt, N. Pojskić, M. Wiens, V. Gamulin & W. E. G. Müller, 2008. Mitochondrial genome of Suberites domuncula: Palindromes and inverted repeats are abundant in non-coding regions. Gene 412: 1–11.PubMedCrossRefGoogle Scholar
  31. Manconi, R. & R. Pronzato, 2002. Suborder Spongillina subord. nov: Freshwater sponges. In Hooper, J. N. A. & R. W. M. van Soest (eds), Systema Porifera: A Guide to the Classification of Sponges. Kluwer, New York: 921–1019.Google Scholar
  32. Meixner, M. J., C. Lüter, C. Eckert, V. Itskovich, D. Janussen, T. von Rintelen, A. V. Bohne, J. M. Meixner & W. R. Hess, 2007. Phylogenetic analysis of freshwater sponges provide evidence for endemism and radiation in ancient lakes. Molecular Phylogenetics and Evolution 45: 875–886.PubMedCrossRefGoogle Scholar
  33. Nedelcu, A. M. & R. W. Lee, 1998. Short repetitive sequences in green algal mitochondrial genomes: potential roles in mitochondrial genome evolution. Molecular Biology and Evolution 15: 690–701.PubMedGoogle Scholar
  34. Paquin, B., M. J. Laforest & B. F. Lang, 2000. Double-hairpin elements in the mitochondrial DNA of allomyces. Molecular Biology and Evolution 17: 1760–1768.PubMedGoogle Scholar
  35. Peterson, K. J. & N. J. Butterfield, 2005. Origin of the Eumetazoa: testing ecological predictions of molecular clocks against the Proterozoic fossil record. Proceedings of the National Academy of Sciences USA 102: 9547–9552.CrossRefGoogle Scholar
  36. Rice, P., I. Longden & A. Bleasby, 2000. EMBOSS: the European Molecular Biology Open Software Suite. Trends in Genetics 16: 276–277.PubMedCrossRefGoogle Scholar
  37. Rosengarten, R. D., E. A. Sperling, M. A. Moreno, S. P. Leys & S. L. Dellaporta, 2008. The mitochondrial genome of the hexactinellid sponge Aphrocallistes vastus: evidence for programmed translational frameshifting. BMC Genomics 9: 33.PubMedCrossRefGoogle Scholar
  38. Saito, S., K. Tamura & T. Aotsuka, 2005. Replication origin of mitochondrial DNA in insects. Genetics 171: 1695–1705.PubMedCrossRefGoogle Scholar
  39. Sanderson, M. J., 2003. r8 s; inferring absolute rates of evolution and divergence times in the absence of a molecular clock. Bioinformatics 19: 301–302.PubMedCrossRefGoogle Scholar
  40. Shao, Z., S. Graf, O. Y. Chaga & D. V. Lavrov, 2006. Mitochondrial genome of the moon jelly Aurelia aurita (Cnidaria, Scyphozoa): a linear DNA molecule encoding a putative DNA-dependent DNA polymerase. Gene 381: 92–101.PubMedCrossRefGoogle Scholar
  41. Sket, B. & M. Velikonja, 1984. Prethodni izvještaj o nalazima slatkovodnih spužvi (Porifera, Spongillidae) u spiljama Jugoslavije, In Deveti jugoslavenski speleološki kongres: 553–557.Google Scholar
  42. Smith, D. R. & R. W. Lee, 2009. The mitochondrial and plastid genomes of Volvox carteri: bloated molecules rich in repetitive DNA. BMC Genomics 10: 132.PubMedCrossRefGoogle Scholar
  43. Swofford, D. L., 2000. PAUP: Phylogenetic Analysis Using Parsimony (and Other Methods), Version 4.0. Sinauer, Sunderland.Google Scholar
  44. Thompson, J. D., D. G. Higgins & T. J. Gibson, 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22: 4673–4680.PubMedCrossRefGoogle Scholar
  45. Veynberg, E., 2009. Fossil sponge fauna in lake baikal region. Progress in Molecular and Subcellular Biology 47: 185–205.PubMedCrossRefGoogle Scholar
  46. Wagner, E., 1991. Herpesvirus Transcription and its Regulation. CRC Press, Boca Raton.Google Scholar
  47. Wang, X. & D. V. Lavrov, 2008. Seventeen new complete mtDNA sequences reveal extensive mitochondrial genome evolution within the Demospongiae. Plos ONE 3(7): e2723.PubMedCrossRefGoogle Scholar
  48. Weinberg, E., I. Weinberg, S. Efremova, A. Tanichev & Y. Masuda, 2003. Late Pliocene spongial fauna in Lake Baikal (from material from the Deep Drilling Core BDP-96–1). In Kashiwaya, K. (ed.), Long Continental Records from Lake Baikal. Springer-Verlag, Tokyo: 283–293.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Bruna Pleše
    • 1
    Email author
  • Lada Lukić-Bilela
    • 2
    • 3
  • Branka Bruvo-Mađarić
    • 1
  • Matija Harcet
    • 1
  • Mirna Imešek
    • 1
  • Helena Bilandžija
    • 1
  • Helena Ćetković
    • 1
    Email author
  1. 1.Department of Molecular BiologyRuđer Bošković InstituteZagrebCroatia
  2. 2.Institute for Genetic Engineering and BiotechnologySarajevoBosnia and Herzegovina
  3. 3.Department of Biology, Faculty of ScienceUniversity of SarajevoSarajevoBosnia and Herzegovina

Personalised recommendations